Plant defense resistance in natural enemies of a specialist insect herbivore
Autor: | Chad Nielson, Christelle A. M. Robert, Carla C. M. Arce, Lingfei Hu, Bruce E. Hibbard, Sandra Gruenig, Matthias Erb, Ricardo A. R. Machado, Maxime R. Hervé, Christian Parisod, Cong van Doan, Xi Zhang |
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Přispěvatelé: | University of Bern, ARS, Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Institut National de la Recherche Agronomique (INRA)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, 157884, Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung, USDA-ARS : Agricultural Research Service, Institut National de la Recherche Agronomique (INRA)-Université de Rennes (UR)-AGROCAMPUS OUEST, Université de Rennes 1 (UR1), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) |
Jazyk: | angličtina |
Rok vydání: | 2019 |
Předmět: |
0106 biological sciences
0301 basic medicine Biocontrôle Biological pest control biological control Insect 580 Plants (Botany) natural enemies Western corn rootworm 01 natural sciences Predation Rhabditida coevolutionary arms race plant secondary metabolism plant–herbivore interactions tritrophic interactions Plant defense against herbivory Plant secondary metabolism media_common 2. Zero hunger chrysomele du mais Multidisciplinary Ecology biology food and beverages Biological Sciences Coleoptera ennemi naturel nématode entomopathogène insect nematodes Food Chain media_common.quotation_subject metabolite herbivore Zea mays Host-Parasite Interactions 03 medical and health sciences Evolutionary arms race Animals Herbivory défense de la plante Herbivore fungi 15. Life on land biology.organism_classification Benzoxazines [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology 030104 developmental biology [SDE.BE]Environmental Sciences/Biodiversity and Ecology contrôle biologique 010606 plant biology & botany [SDV.EE.IEO]Life Sciences [q-bio]/Ecology environment/Symbiosis |
Zdroj: | Proceedings of the National Academy of Sciences of the United States of America Proceedings of the National Academy of Sciences of the United States of America, National Academy of Sciences, 2019, 116 (46), pp.23174-23181. ⟨10.1073/pnas.1912599116⟩ Proceedings of the National Academy of Sciences of the United States of America, 2019, 116 (46), pp.23174-23181. ⟨10.1073/pnas.1912599116⟩ Zhang, Xi; van Doan, Cong; Arce, Carla C. M.; Hu, Lingfei; Gruenig, Sandra; Parisod, Christian; Hibbard, Bruce E.; Hervé, Maxime R.; Nielson, Chad; Robert, Christelle A. M.; Machado, Ricardo A. R.; Erb, Matthias (2019). Plant defense resistance in natural enemies of a specialist insect herbivore. Proceedings of the National Academy of Sciences of the United States of America-PNAS, 116(46), pp. 23174-23181. National Academy of Sciences NAS 10.1073/pnas.1912599116 |
ISSN: | 0027-8424 1091-6490 |
DOI: | 10.1073/pnas.1912599116⟩ |
Popis: | Significance Certain adapted insect herbivores utilize plant toxins for self-defense against their own enemies. These adaptations structure ecosystems and limit our capacity to use biological control agents to manage specialized agricultural pests. We show that entomopathogenic nematodes that are exposed to the western corn rootworm, an important agricultural pest that sequesters defense metabolites from maize, can evolve resistance to these defenses. Resisting the plant defense metabolites likely allows the nematodes to infect and kill the western corn rootworm more efficiently. These findings illustrate how predators can counter the plant-based resistance strategies of specialized insect herbivores. Breeding or engineering biological control agents that resist plant defense metabolites may improve their capacity to kill important agricultural pests such as the western corn rootworm. Plants defend themselves against herbivores through the production of toxic and deterrent metabolites. Adapted herbivores can tolerate and sometimes sequester these metabolites, allowing them to feed on defended plants and become toxic to their own enemies. Can herbivore natural enemies overcome sequestered plant defense metabolites to prey on adapted herbivores? To address this question, we studied how entomopathogenic nematodes cope with benzoxazinoid defense metabolites that are produced by grasses and sequestered by a specialist maize herbivore, the western corn rootworm. We find that nematodes from US maize fields in regions in which the western corn rootworm was present over the last 50 y are behaviorally and metabolically resistant to sequestered benzoxazinoids and more infective toward the western corn rootworm than nematodes from other parts of the world. Exposure of a benzoxazinoid-susceptible nematode strain to the western corn rootworm for 5 generations results in higher behavioral and metabolic resistance and benzoxazinoid-dependent infectivity toward the western corn rootworm. Thus, herbivores that are exposed to a plant defense sequestering herbivore can evolve both behavioral and metabolic resistance to plant defense metabolites, and these traits are associated with higher infectivity toward a defense sequestering herbivore. We conclude that plant defense metabolites that are transferred through adapted herbivores may result in the evolution of resistance in herbivore natural enemies. Our study also identifies plant defense resistance as a potential target for the improvement of biological control agents. |
Databáze: | OpenAIRE |
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